Ultrastructural and functional characterization of satellitosis in the human lateral amygdala associated with Ammon’s horn sclerosis

Abstract

The amygdala displays neuronal cell loss and gliosis in human temporal lobe epilepsy (TLE). Therefore, we investigated a certain type of gliosis, called satellitosis, in the lateral amygdala (LA) of TLE patients with Ammon's horn sclerosis (AHS, n = 15) and non-AHS (n = 12), and in autopsy controls. Satellite cells were quantified using light and electron microscopy at the somata of Nissl-stained and glutamic acid decarboxylase-negative projection neurons, and their functional properties were studied using electrophysiology. Non-AHS cases suffered from ganglioglioma, cortical dysplasia, Sturge-Weber syndrome, astrocytoma WHO III-IV, Rasmussen's encephalitis, cerebral infarction and perinatal brain damage. TLE cases with AHS had a more prominent satellitosis as compared to non-AHS and/or autopsy cases, which correlated with epilepsy duration but not age. At ultrastructural level, the predominant type of satellite cells occurring in both AHS and non-AHS cases displayed a dark cytoplasm and an irregularly shaped dark nucleus, whereas perineuronal glial cells with a light cytoplasm and light oval nucleus were much rarer. Satellite cells expressed time- and voltage-dependent transmembrane currents as revealed by patch-clamp recordings typical for 'complex' glia, although only 44% of satellite cells were immunostained for the chondroitin sulfate proteoglycan NG2. Together, the perineuronal cells described here were a heterogenous cell population regarding their NG2 expression, although they resembled NG2 cells rather than bona fide oligodendrocytes and astrocytes based on their ultrastructural and electrophysiological characteristics. Thus, perineuronal satellitosis as studied in the LA seems to be a hallmark of AHS-associated TLE pathology in patients suffering from intractable epilepsy.